Ex vivo Dynamics of Human Glioblastoma Cells in a Microvasculature‐on‐a‐Chip System Correlates with Tumor Heterogeneity and Subtypes
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Abstract
The perivascular niche (PVN) plays an essential role in brain tumor stem‐like cell (BTSC) fate control, tumor invasion, and therapeutic resistance. Here, a microvasculature‐on‐a‐chip system as a PVN model is used to evaluate the ex vivo dynamics of BTSCs from ten glioblastoma patients. BTSCs are found to preferentially localize in the perivascular zone, where they exhibit either the lowest motility, as in quiescent cells, or the highest motility, as in the invasive phenotype, with migration over long distance. These results indicate that PVN is a niche for BTSCs, while the microvascular tracks may serve as a path for tumor cell migration. The degree of colocalization between tumor cells and microvessels varies significantly across patients. To validate these results, single‐cell transcriptome sequencing (10 patients and 21 750 single cells in total) is performed to identify tumor cell subtypes. The colocalization coefficient is found to positively correlate with proneural (stem‐like) or mesenchymal (invasive) but not classical (proliferative) tumor cells. Furthermore, a gene signature profile including PDGFRA correlates strongly with the “homing” of tumor cells to the PVN. These findings demonstrate that the model can recapitulate in vivo tumor cell dynamics and heterogeneity, representing a new route to study patient‐specific tumor cell functions.
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The perivascular niche (PVN) is a niche for brain tumor stem-like cells (BTSCs).
“It was found that the PVN is a niche for BTSCs, and the microvascular diameter can be used as a pathway for tumor metastasis.”
From Tumor-on-a-chip: from bioinspired design to biomedical application (2021) · cites this paper as [196]
The microvascular diameter can be used as a pathway for tumor metastasis.
“It was found that the PVN is a niche for BTSCs, and the microvascular diameter can be used as a pathway for tumor metastasis.”
From Tumor-on-a-chip: from bioinspired design to biomedical application (2021) · cites this paper as [196]
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Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
Verhaak, R. G. W., Hoadley, K. A., Purdom, E., Wang, V., Qi, Y., Wilkerson, M. D., Miller, C. R., Ding, L., Golub, T., Mesirov, J. P., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2009.12.020 · Cited by 7,575 · see citing works
Trapnell, C., Cacchiarelli, D., Grimsby, J., Pokharel, P., Li, S., Morse, M., Lennon, N. J., Livak, K. J., Mikkelsen, T. S., & Rinn, J. L. (2014) · Nature Biotechnology · doi:10.1038/nbt.2859 · Cited by 7,314 · see citing works
Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets.
Macosko, E. Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A. R., Kamitaki, N., Martersteck, E. M., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.002 · Cited by 7,110 · see citing works
Spatial reconstruction of single-cell gene expression data
Satija, R., Farrell, J. A., Gennert, D., Schier, A. F., & Regev, A. (2015) · Nature Biotechnology · doi:10.1038/nbt.3192 · Cited by 7,055 · see citing works
Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma
Patel, A. P., Tirosh, I., Trombetta, J. J., Shalek, A. K., Gillespie, S. M., Wakimoto, H., Cahill, D. P., Nahed, B. V., Curry, W. T., Martuza, R. L., et al. (2014) · Science · doi:10.1126/science.1254257 · Cited by 5,063 · see citing works
The Somatic Genomic Landscape of Glioblastoma
Brennan, C. W., Verhaak, R. G. W., McKenna, A., Campos, B., Noushmehr, H., Salama, S. R., Zheng, S., Chakravarty, D., Sanborn, J. Z., Berman, S. H., et al. (2013) · Cell · doi:10.1016/j.cell.2013.09.034 · Cited by 5,016 · see citing works
Self-citationPHILLIPS, H. S., Kharbanda, S., Chen, R., Forrest, W. F., Soriano, R. H., Wu, T. D., Misra, A., Nigro, J. M., Colman, H., Soroceanu, L., et al. (2006) · Cancer Cell · doi:10.1016/j.ccr.2006.02.019 · Cited by 3,106 · see citing works
Advances in engineering hydrogels
Zhang, Y. S., & Khademhosseini, A. (2017) · Science · doi:10.1126/science.aaf3627 · Cited by 2,908 · see citing works
Isolation and Characterization of Tumorigenic, Stem-like Neural Precursors from Human Glioblastoma
Galli, R., Binda, E., Orfanelli, U., Cipelletti, B., Gritti, A., Vitis, S. D., Fiocco, R., Foroni, C., DiMeco, F., & Vescovi, A. L. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-1364 · Cited by 2,570 · see citing works
Lee, J., Kotliarova, S. E., Kotliarov, Y., Li, A., Su, Q., Donin, N. M., Pastorino, S., Purow, B. W., Christopher, N., Zhang, W., et al. (2006) · Cancer Cell · doi:10.1016/j.ccr.2006.03.030 · Cited by 2,289 · see citing works
Capturing complex 3D tissue physiology in vitro
Griffith, L. G., & Swartz, M. A. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1858 · Cited by 2,274 · see citing works
A Perivascular Niche for Brain Tumor Stem Cells
Calabrese, C. R., Poppleton, H., Koçak, M., Hogg, T. L., Fuller, C. E., Hamner, J. B., Oh, E. Y., Gaber, M. W., Finklestein, D., Allen, M., et al. (2007) · Cancer Cell · doi:10.1016/j.ccr.2006.11.020 · Cited by 2,203 · see citing works
Extracellular Vesicles in Cancer: Cell-to-Cell Mediators of Metastasis
Becker, A., Thakur, B. K., Weiss, J. M., Kim, H. S., Peinado, H., & Lyden, D. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.10.009 · Cited by 2,003 · see citing works
A practical guide to evaluating colocalization in biological microscopy.
Dunn, K., Kamocka, M., & McDonald, J. (2011) · American Journal of Physiology - Cell Physiology · doi:10.1152/ajpcell.00462.2010 · Cited by 1,998 · see citing works
Wang, Q., Hu, B., Hu, X., Kim, H., Squatrito, M., Scarpace, L. M., deCarvalho, A. C., Lyu, S., Li, P., Li, Y., et al. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.06.003 · Cited by 1,975 · see citing works
Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues
Miller, J. S., Stevens, K. R., Yang, M. T., Baker, B. M., Nguyen, D.-H. T., Cohen, D. M., Toro, E., Chen, A. A., Galie, P. A., Yu, X., et al. (2012) · Nature Materials · doi:10.1038/nmat3357 · Cited by 1,917 · see citing works
Self-citationSingle-cell mRNA quantification and differential analysis with Census
Qiu, X., Hill, A. J., Packer, J. S., Lin, D., Ma, Y.-A., & Trapnell, C. (2017) · Nature Methods · doi:10.1038/nmeth.4150 · Cited by 1,885 · see citing works
Cell and environment interactions in tumor microregions: the multicell spheroid model.
Sutherland, R. M. (1988) · Science · doi:10.1126/science.2451290 · Cited by 1,803 · see citing works
Modeling Tissue Morphogenesis and Cancer in 3D
Yamada, K. M., & Cukierman, E. (2007) · Cell · doi:10.1016/j.cell.2007.08.006 · Cited by 1,751 · see citing works
Cancer stem cells in glioblastomaPreprint
Lathia, J. D., Mack, S. C., Mulkearns-Hubert, E. E., Valentim, C. L. L., & Rich, J. N. (2015) · Genes & Development · doi:10.1101/gad.261982.115 · Cited by 1,600 · see citing works
Three-dimensional in vitro cell culture models in drug discovery and drug repositioning
Langhans, S. A. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00006 · Cited by 1,522 · see citing works
Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells
Ricci‐Vitiani, L., Pallini, R., Biffoni, M., Todaro, M., Invernici, G., Cenci, T., Maira, G., Parati, E. A., Stassi, G., Larocca, L. M., et al. (2010) · Nature · doi:10.1038/nature09557 · Cited by 1,378 · see citing works
Glioblastoma stem-like cells give rise to tumour endothelium
Wang, R., Chadalavada, K., Wilshire, J. A., Kowalik, U., Hovinga, K. E., Geber, A. B., Fligelman, B., Leversha, M. A., Brennan, C., & Tabar, V. S. (2010) · Nature · doi:10.1038/nature09624 · Cited by 1,203 · see citing works
Three-dimensional culture systems in cancer research: Focus on tumor spheroid model
Nath, S., & Devi, G. R. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.03.013 · Cited by 919 · see citing works
Glioblastoma Stem Cells Generate Vascular Pericytes to Support Vessel Function and Tumor Growth
Cheng, L., Huang, Z., Zhou, W., Wu, Q., Donnola, S., Liu, J. K., Fang, X., Sloan, A. E., Mao, Y., Lathia, J. D., et al. (2013) · Cell · doi:10.1016/j.cell.2013.02.021 · Cited by 905 · see citing works
Self-citationIn vitro microvessels for the study of angiogenesis and thrombosis
Zheng, Y., Chen, J., Craven, M., Choi, N. W., Totorica, S., Diaz-Santana, A., Kermani, P., Hempstead, B., Fischbach-Teschl, C., López, J. A., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201240109 · Cited by 894 · see citing works
Three-dimensional microfluidic model for tumor cell intravasation and endothelial barrier function
Zervantonakis, I. K., Hughes-Alford, S. K., Charest, J. L., Condeelis, J. S., Gertler, F. B., & Kamm, R. D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210182109 · Cited by 872 · see citing works
Engineering of functional, perfusable 3D microvascular networks on a chip
Kim, S., Lee, H., Chung, M., & Jeon, N. L. (2013) · Lab on a Chip · doi:10.1039/c3lc41320a · Cited by 872 · see citing works
Three-Dimensional Cell Cultures in Drug Discovery and Development
Fang, Y., & Eglen, R. M. (2017) · SLAS Discovery · doi:10.1177/1087057117696795 · Cited by 849 · see citing works
Comparison of 2D- and 3D-culture models as drug-testing platforms in breast cancer
IMAMURA, Y., MUKOHARA, T., SHIMONO, Y., FUNAKOSHI, Y., CHAYAHARA, N., TOYODA, M., KIYOTA, N., TAKAO, S., KONO, S., NAKATSURA, T., et al. (2015) · Oncology Reports · doi:10.3892/or.2015.3767 · Cited by 845 · see citing works
A neurocentric perspective on glioma invasion
Cuddapah, V. A., Robel, S., Watkins, S., & Sontheimer, H. W. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3765 · Cited by 826 · see citing works
Human 3D vascularized organotypic microfluidic assays to study breast cancer cell extravasation
Jeon, J. S., Bersini, S., Gilardi, M., Dubini, G., Charest, J. L., Moretti, M., & Kamm, R. D. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1417115112 · Cited by 723 · see citing works
Making a tumour's bed: glioblastoma stem cells and the vascular niche
Gilbertson, R. J., & Rich, J. N. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2246 · Cited by 716 · see citing works
Tumor microvasculature and microenvironment: Targets for anti-angiogenesis and normalization
Fukumura, D., & Jain, R. K. (2007) · Microvascular Research · doi:10.1016/j.mvr.2007.05.003 · Cited by 699 · see citing works
Rong, Y., Durden, D. L., Meir, E. G. V., & Brat, D. J. (2006) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-200606000-00001 · Cited by 564 · see citing works
Formation of perfused, functional microvascular tubes in vitro
Chrobak, K. M., Potter, D. R., & Tien, J. (2006) · Microvascular Research · doi:10.1016/j.mvr.2006.02.005 · Cited by 555 · see citing works
Disruption of astrocyte–vascular coupling and the blood–brain barrier by invading glioma cells
Watkins, S., Robel, S., Kimbrough, I. F., Robert, S. M., Ellis‐Davies, G. C. R., & Sontheimer, H. W. (2014) · Nature Communications · doi:10.1038/ncomms5196 · Cited by 551 · see citing works
Charles, N., Ozawa, T., Squatrito, M., Bleau, A.-M., Brennan, C. W., Hambardzumyan, D., & Holland, E. C. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.01.001 · Cited by 550 · see citing works
Glioblastoma: defining tumor niches
Hambardzumyan, D., & Bergers, G. (2015) · Trends in Cancer · doi:10.1016/j.trecan.2015.10.009 · Cited by 522 · see citing works
Biomimetic model to reconstitute angiogenic sprouting morphogenesis in vitro
Nguyen, D.-H. T., Stapleton, S. C., Yang, M. T., Cha, S. S., Choi, C. K., Galie, P. A., & Chen, C. S. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1221526110 · Cited by 487 · see citing works
Tumor Organoids as a Pre-clinical Cancer Model for Drug Discovery
Weeber, F., Ooft, S., Dijkstra, K. K., & Voest, E. E. (2017) · Cell chemical biology · doi:10.1016/j.chembiol.2017.06.012 · Cited by 486 · see citing works
Günther, H. S., Schmidt, N. O., PHILLIPS, H. S., Kemming, D., Kharbanda, S., Soriano, R. H., Modrusan, Z. D., Meissner, H., Westphal, M., & Lamszus, K. (2007) · Oncogene · doi:10.1038/sj.onc.1210949 · Cited by 443 · see citing works
Glioblastoma targeted therapy: updated approaches from recent biological insights
Touat, M., Idbaïh, A., Sanson, M., & Ligon, K. L. (2017) · Annals of Oncology · doi:10.1093/annonc/mdx106 · Cited by 443 · see citing works
<i>In Vitro</i> Perfused Human Capillary Networks
Moya, M. L., Hsu, Y.-H., Lee, A. P., Hughes, C. C. W., & George, S. C. (2013) · Tissue Engineering Part C: Methods · doi:10.1089/ten.tec.2012.0430 · Cited by 387 · see citing works
3D microtumors in vitro supported by perfused vascular networks
Sobrino, A., Phan, D. T. T., Datta, R., Wang, X., Hachey, S. J., Romero-López, M., Gratton, E., Lee, A. P., George, S. C., & Hughes, C. C. W. (2016) · Scientific Reports · doi:10.1038/srep31589 · Cited by 387 · see citing works
Chen, M. B., Whisler, J. A., Fröse, J., Yu, C., Shin, Y., & Kamm, R. D. (2017) · Nature Protocols · doi:10.1038/nprot.2017.018 · Cited by 385 · see citing works
Most Human Non-GCIMP Glioblastoma Subtypes Evolve from a Common Proneural-like Precursor Glioma
Ozawa, T., Riester, M., Cheng, Y.-K., Huse, J. T., Squatrito, M., Helmy, K. Y., Charles, N. A., Michor, F., & Holland, E. C. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.06.005 · Cited by 382 · see citing works
Histopathology, classification, and grading of gliomas
Kleihues, P., Söylemezoğlu, F., Schäuble, B., Scheithauer, B. W., & Burger, P. C. (1995) · Glia · doi:10.1002/glia.440150303 · Cited by 358 · see citing works
A vascularized and perfused organ-on-a-chip platform for large-scale drug screening applications
Phan, D. T. T., Wang, X., Craver, B. M., Sobrino, A., Zhao, D., Chen, J. C., Lee, L. Y. N., George, S. C., Lee, A. P., & Hughes, C. C. W. (2017) · Lab on a Chip · doi:10.1039/c6lc01422d · Cited by 325 · see citing works
Structural Development in Gliomas
Scherer, H.-J. (1938) · American Journal of Cancer · doi:10.1158/ajc.1938.333 · Cited by 322 · see citing works
Tsai, M., Kita, A., Leach, J., Rounsevell, R., Huang, J. N., Moake, J., Ware, R. E., Fletcher, D. A., & Lam, W. A. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58753 · Cited by 297 · see citing works
Dura, B., Choi, J.-Y., Zhang, K., Damsky, W., Thakral, D., Bosenberg, M., Craft, J. E., & Fan, R. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky1173 · Cited by 285 · see citing works
Self-citationGlioblastoma stem‐like cells secrete the pro‐angiogenic VEGF‐A factor in extracellular vesicles
Treps, L., Perret, R. E., Edmond, S., Ricard, D., & Gavard, J. (2017) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2017.1359479 · Cited by 276 · see citing works
Dønnem, T., Hu, J., Ferguson, M. L., Adighibe, O., Snell, C. E., Harris, A. L., Gatter, K. C., & Pezzella, F. (2013) · Cancer Medicine · doi:10.1002/cam4.105 · Cited by 275 · see citing works
Highly penetrative, drug-loaded nanocarriers improve treatment of glioblastoma
Zhou, J., Patel, T., Sirianni, R. W., Strohbehn, G. W., Zheng, M., Duong, N. T., Schafbauer, T., Huttner, A. J., Huang, Y. H., Carson, R. E., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1304504110 · Cited by 272 · see citing works
Self-citationTargeting adaptive glioblastoma: an overview of proliferation and invasion
Xie, Q. R., Mittal, S., & Berens, M. E. (2014) · Neuro-Oncology · doi:10.1093/neuonc/nou147 · Cited by 258 · see citing works
Control of Perfusable Microvascular Network Morphology Using a Multiculture Microfluidic System
Whisler, J. A., Chen, M. B., & Kamm, R. D. (2012) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2013.0370 · Cited by 240 · see citing works
Single-cell transcriptome analysis of lineage diversity in high-grade glioma
Yuan, J., Levitin, H. M., Frattini, V., Bush, E. C., Boyett, D. M., Samanamud, J. L., Ceccarelli, M., Dovas, A., Zanazzi, G. J., Canoll, P., et al. (2018) · Genome Medicine · doi:10.1186/s13073-018-0567-9 · Cited by 237 · see citing works
Jeon, J. S., Bersini, S., Whisler, J. A., Chen, M. B., Dubini, G., Charest, J. L., Moretti, M., & Kamm, R. D. (2014) · Integrative Biology · doi:10.1039/c3ib40267c · Cited by 229 · see citing works
di Tomaso, E., Snuderl, M., Kamoun, W. S., Duda, D. G., Auluck, P. K., Fazlollahi, L., Andronesi, O. C., Frosch, M. P., Wen, P. Y., Plotkin, S. R., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-2602 · Cited by 200 · see citing works
A three-dimensional in vitro model of tumor cell intravasation
Ehsan, S. M., Welch-Reardon, K. M., Waterman, M. L., Hughes, C. C. W., & George, S. C. (2014) · Integrative Biology · doi:10.1039/c3ib40170g · Cited by 196 · see citing works
The perivascular niche microenvironment in brain tumor progression
Charles, N. A., & Holland, E. C. (2010) · Cell Cycle · doi:10.4161/cc.9.15.12710 · Cited by 193 · see citing works
Hsu, Y., Moya, M. L., Hughes, C. C. W., George, S. C., & Lee, A. P. (2013) · Lab on a Chip · doi:10.1039/c3lc50424g · Cited by 192 · see citing works
A CRITICAL REVIEW: THE PATHOLOGY OF CEREBRAL GLIOMAS
Scherer, H.-J. (1940) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.3.2.147 · Cited by 192 · see citing works
The cancer stem cell niche(s): The crosstalk between glioma stem cells and their microenvironment
Filatova, A., Acker, T., & Garvalov, B. K. (2012) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2012.10.008 · Cited by 166 · see citing works
Dresemann, G. P., Weller, M., Rosenthal, M. A., Wedding, U., Wagner, W., Engel, E., Heinrich, B., Mayer‐Steinacker, R., Krarup‐Hansen, A., Fluge, Ø., et al. (2009) · Journal of Neuro-Oncology · doi:10.1007/s11060-009-9976-3 · Cited by 156 · see citing works
Baker, G. J., Yadav, V. N., Motsch, S., Koschmann, C. J., Calinescu, A., Mineharu, Y., Camelo-Piragua, S. I., Orringer, D. A., Bannykh, S., Nichols, W. S., et al. (2014) · Neoplasia · doi:10.1016/j.neo.2014.06.003 · Cited by 155 · see citing works
A 3D Fibrous Scaffold Inducing Tumoroids: A Platform for Anticancer Drug Development
Girard, Y., Wang, C., Ravi, S., Howell, M., Mallela, J. P., Alibrahim, M., Green, R. J., Hellermann, G., Mohapatra, S. S., & Mohapatra, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075345 · Cited by 134 · see citing works
Reardon, D. A., Dresemann, G. P., Taillibert, S., Campone, M., van den Bent, M. J., Clément, P. M., Blomquist, E., Gordower, L., Schultz, H., Raizer, J. J., et al. (2009) · British Journal of Cancer · doi:10.1038/sj.bjc.6605411 · Cited by 132 · see citing works
Extracellular Vesicles in Brain Tumors and Neurodegenerative Diseases
Ciregia, F., Urbani, A., & Palmisano, G. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00276 · Cited by 110 · see citing works
HONG, X., Chedid, K., & Kalkanis, S. N. (2012) · International Journal of Oncology · doi:10.3892/ijo.2012.1592 · Cited by 101 · see citing works
Genetic modeling of gliomas in mice: New tools to tackle old problems
Hambardzumyan, D., Parada, L. F., Holland, E. C., & Charest, A. (2011) · Glia · doi:10.1002/glia.21142 · Cited by 99 · see citing works
Ayuso, J. M., Monge, R., Martínez‐González, A., Virumbrales-Muñoz, M., Llamazares, G. A., Berganzo, J., Hernández‐Laín, A., Santolaria, J., Doblaré, M., Hubert, C. G., et al. (2016) · Neuro-Oncology · doi:10.1093/neuonc/now230 · Cited by 95 · see citing works
Huang, Y.-J., & Hsu, S. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.09.010 · Cited by 77 · see citing works
Alvetex®: Polystyrene Scaffold Technology for Routine Three Dimensional Cell Culture
Knight, E., Murray, B. A., Carnachan, R. J., & Przyborski, S. A. (2010) · Methods in molecular biology · doi:10.1007/978-1-60761-984-0_20 · Cited by 75 · see citing works
Key concepts in glioblastoma therapy
Bartek, J. J., Ng, K., Bartek, J. J., Fischer, W., Carter, B. S., & Chen, C. C. (2012) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2011-300709 · Cited by 72 · see citing works
Stadler, M., Walter, S., Walzl, A., Kramer, N., Unger, C., Scherzer, M., Unterleuthner, D., Hengstschläger, M., Krupitza, G., & Dolznig, H. (2015) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2015.08.007 · Cited by 70 · see citing works
Permeability of single capillaries to intermediate-sized colored solutes
CURRY, F. E., Huxley, V. H., & Adamson, R. H. (1983) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1983.245.3.h495 · Cited by 50 · see citing works
Hitting Them Where They Live: Targeting the Glioblastoma Perivascular Stem Cell Niche
Brooks, M. D., Sengupta, R., Snyder, S. C., & Rubin, J. B. (2013) · Current Pathobiology Reports · doi:10.1007/s40139-013-0012-0 · Cited by 41 · see citing works
A Novel Flow Bioreactor for In Vitro Microvascularization
Lee, E. J., & Niklason, L. E. (2010) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2009.0652 · Cited by 38 · see citing works
Optimization of radiation dosing schedules for proneural glioblastoma
Badri, H., Pitter, K. L., Holland, E. C., Franziska Michor, A., & Leder, K. (2015) · Journal of Mathematical Biology · doi:10.1007/s00285-015-0908-x · Cited by 35 · see citing works
Li, X., Xu, S., He, P., & Liu, Y. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126797 · Cited by 34 · see citing works
Filopodial Morphology Correlates to the Capture Efficiency of Primary T-Cells on Nanohole Arrays
Kim, D.-J., Kim, G., Seol, J.-K., Hyung, J.-H., Park, N., Lee, M.-R., Lee, M. K., Fan, R., & Lee, S. (2013) · Journal of Biomedical Nanotechnology · doi:10.1166/jbn.2014.1814 · Cited by 8 · see citing works
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- [8]T. Donnem, J. Hu, M. Ferguson, O. Adighibe, C. Snell, A. L. Harris, K. C. Gatter, F. Pezzella, Cancer Med. 2013, 2, 427. 24156015 PMC3799277
- [9]H. J. Scherer, Am. J. Cancer 1938, 34, 333.
- [20]Y. Fang, R. M. Eglen, SLAS Discovery 2017, 22, 456. 28520521 PMC5448717
- [74]C. W. Brennan, R. G. Verhaak, A. McKenna, B. Campos, H. Noushmehr, S. R. Salama, S. Zheng, D. Chakravarty, J. Z. Sanborn, S. H. Berman, R. Beroukhim, B. Bernard, C. J. Wu, G. Genovese, I. Shmulevich, J. Barnholtz‐Sloan, L. Zou, R. Vegesna, S. A. Shukla, G. Ciriello, W. K. Yung, W. Zhang, C. Sougnez, T. Mikkelsen, K. Aldape, D. D. Bigner, E. G. Van Meir, M. Prados, A. Sloan, K. L. Black, J. Eschbacher, G. Finocchiaro, W. Friedman, D. W. Andrews, A. Guha, M. Iacocca, B. P. O'Neill, G. Foltz, J. Myers, D. J. Weisenberger, R. Penny, R. Kucherlapati, C. M. Perou, D. N. Hayes, R. Gibbs, M. Marra, G. B. Mills, E. Lander, P. Spellman, R. Wilson, C. Sander, J. Weinstein, M. Meyerson, S. Gabriel, P. W. Laird, D. Haussler, G. Getz, L. Chin, T. R. Network, Cell 2013, 155, 462.24120142
- [81]E. J. Lee, L. E. Niklason, Tissue Eng., Part C 2010, 16, 1191. PMC2943404 20170423
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Applications of single-cell sequencing in cancer research: progress and perspectives
Lei, Y., Tang, R., Xu, J., Wang, W., Zhang, B., Liu, J., Yu, X., & Shi, S. (2021) · Journal of Hematology & Oncology · doi:10.1186/s13045-021-01105-2 · Cited by 597 · see citing works
Self-citationOrgan-on-a-Chip: A New Paradigm for Drug Development
Ma, C., Peng, Y., Li, H., & Chen, W. (2020) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2020.11.009 · Cited by 589 · see citing works
Self-citationLi, S., Su, W., Wu, H., Yuan, T., Yuan, C., Liu, J., Deng, G., Gao, X., Chen, Z., Bao, Y., et al. (2020) · Nature Biomedical Engineering · doi:10.1038/s41551-020-0540-y · Cited by 425 · see citing works
Self-citationTumor-on-a-chip: from bioinspired design to biomedical application
Liu, X., Fang, J., Huang, S., Wu, X., Xie, X., Wang, J., Liu, F., Zhang, M., Peng, Z., & Hu, N. (2021) · Microsystems & Nanoengineering · doi:10.1038/s41378-021-00277-8 · Cited by 246 · see citing works
Cui, X., Ma, C., Vasudevaraja, V., Serrano, J., Tong, J., Peng, Y., DeLorenzo, M., Shen, G., Frenster, J. D., Morales, R. T., et al. (2020) · eLife · doi:10.7554/elife.52253 · Cited by 163 · see citing works
Dissecting and rebuilding the glioblastoma microenvironment with engineered materials
Wolf, K. J., Chen, J., Coombes, J. D., Aghi, M. K., & Kumar, S. (2019) · Nature Reviews Materials · doi:10.1038/s41578-019-0135-y · Cited by 159 · see citing works
Endothelial Regulation of Drug Transport in a 3D Vascularized Tumor Model
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Organ‐On‐A‐Chip Models of the Blood–Brain Barrier: Recent Advances and Future Prospects
Kawakita, S., Mandal, K., Mou, L., Mecwan, M. M., Zhu, Y., Li, S., Sharma, S., Hernández, A. L., Nguyen, H. T., Maity, S., et al. (2022) · Small · doi:10.1002/smll.202201401 · Cited by 101 · see citing works
Microfluidic high-throughput 3D cell culture
Ko, J., Park, D., Lee, J., Jung, S., Baek, K., Sung, K. E., Lee, J., & Jeon, N. L. (2024) · Nature Reviews Bioengineering · doi:10.1038/s44222-024-00163-8 · Cited by 88 · see citing works
New Strategy for Promoting Vascularization in Tumor Spheroids in a Microfluidic Assay
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Lim, J., Ching, H., Yoon, J., Jeon, N. L., & Kim, Y. (2021) · Nano Convergence · doi:10.1186/s40580-021-00261-y · Cited by 83 · see citing works
Xiao, Y., Wang, Z., Zhao, M., Deng, Y., Yang, M., Su, G., Yang, K., Qian, C., Hu, X., Liu, Y., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.914236 · Cited by 74 · see citing works
Self-citationRuiz-Garcia, H. J., Alvarado-Estrada, K., Schiapparelli, P. V., Quiñones‐Hinojosa, A., & Trifiletti, D. M. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.558381 · Cited by 75 · see citing works
Angiogenic biomaterials to promote therapeutic regeneration and investigate disease progression
Ngo, M. T., & Harley, B. A. C. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.120207 · Cited by 70 · see citing works
Winkelman, M. A., Kim, D. Y., Kakarla, S., Grath, A., Silvia, N., & Dai, G. (2021) · Lab on a Chip · doi:10.1039/d1lc00605c · Cited by 68 · see citing works
Self-citationPatient‐derived cancer organoids for drug screening: Basic technology and clinical application
Ren, X., Chen, W., Yang, Q., Li, X., & Xu, L. (2022) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.15930 · Cited by 69 · see citing works
Tumor-on-a-chip models combined with mini-tissues or organoids for engineering tumor tissues
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A Dynamic 3D Tumor Spheroid Chip Enables More Accurate Nanomedicine Uptake Evaluation
Zhuang, J., Zhang, J., Wu, M., & Zhang, Y. (2019) · Advanced Science · doi:10.1002/advs.201901462 · Cited by 66 · see citing works
A Robust Method for Perfusable Microvascular Network Formation In Vitro
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Biofabrication Strategies and Engineered In Vitro Systems for Vascular Mechanobiology
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A 3D disease and regeneration model of peripheral nervous system–on–a–chip
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Recent Advances in Microfluidic Platforms for Programming Cell‐Based Living Materials
Zhang, P., Shao, N., & Qin, L. (2021) · Advanced Materials · doi:10.1002/adma.202005944 · Cited by 61 · see citing works
Adjei‐Sowah, E., O’Connor, S. A., Veldhuizen, J., Cascio, C. L., Plaisier, C. L., Mehta, S. V., & Nikkhah, M. (2022) · Advanced Science · doi:10.1002/advs.202201436 · Cited by 59 · see citing works
Glioblastoma-on-a-chip construction and therapeutic applications
Xie, Z., Chen, M., Lian, J., Wang, H., & Ma, J. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1183059 · Cited by 59 · see citing works
Faisal, S. M., Comba, A., Varela, M. L., Argento, A. E., Brumley, E. K., Abel, C. C., Castro, M. G., & Lowenstein, P. R. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1005069 · Cited by 57 · see citing works
Gonzales‐Aloy, E., Ahmed-Cox, A., Tsoli, M., Ziegler, D. S., & Kavallaris, M. (2023) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2023.114777 · Cited by 58 · see citing works
Organ-on-a-chip microengineering for bio-mimicking disease models and revolutionizing drug discovery
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A placenta-on-a-chip model to determine the regulation of FKBPL and galectin-3 in preeclampsia
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Pathophysiology of blood-brain barrier in brain tumor. Novel therapeutic advances using nanomedicine
Sharma, H. S., Muresanu, D. F., Nozari, A., Lafuente, J. V., Tian, Z. R., Sahib, S., Bryukhovetskiy, I., Bryukhovetskiy, A. S., Buzoianu, A. D., Patnaik, R., et al. (2020) · International review of neurobiology · doi:10.1016/bs.irn.2020.03.001 · Cited by 50 · see citing works
Electrophysiology Read-Out Tools for Brain-on-Chip Biotechnology
Forró, C., Caron, D., Angotzi, G. N., Gallo, V., Berdondini, L., Santoro, F., Palazzolo, G., & Panuccio, G. (2021) · Micromachines · doi:10.3390/mi12020124 · Cited by 50 · see citing works
Engineering Organ-on-a-Chip to Accelerate Translational Research
Ko, J., Park, D., Lee, S., Gümüşcü, B., & Jeon, N. L. (2022) · Micromachines · doi:10.3390/mi13081200 · Cited by 52 · see citing works
Slika, H., Karimov, Z., Alimonti, P., Abou‐Mrad, T., Fazio, E. D., Alomari, S., & Tyler, B. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242216316 · Cited by 49 · see citing works
Gerigk, M., Bulstrode, H. J. C. J., Shi, H., Tönisen, F., Cerutti, C., Morrison, G. M., Rowitch, D. H., & Huang, Y. Y. S. (2021) · Lab on a Chip · doi:10.1039/d1lc00271f · Cited by 48 · see citing works
Cancer Models on Chip: Paving the Way to Large‐Scale Trial Applications
Gil, J. F., Moura, C. S., Silvério, V., Gonçalves, G., & Santos, H. A. (2023) · Advanced Materials · doi:10.1002/adma.202300692 · Cited by 45 · see citing works
Zhang, Y., Zhang, B., Lv, C., Zhang, N., Xing, K., Wang, Z., Lv, R., Yu, M., Xu, C., & Wang, Y. (2023) · Theranostics · doi:10.7150/thno.81407 · Cited by 44 · see citing works
Engineering Breast Cancer On-chip—Moving Toward Subtype Specific Models
Moccia, C., & Haase, K. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.694218 · Cited by 34 · see citing works
Cancer-on-a-chip for precision cancer medicine
Liu, L., Wang, H., Chen, R., Song, Y., Wei, W., Baek, D. S. H., Gillin, M., Kurabayashi, K., & Chen, W. (2025) · Lab on a Chip · doi:10.1039/d4lc01043d · Cited by 47 · see citing works
Ayensa-Jiménez, J., Pérez-Aliacar, M., Ranđelović, T., Oliván, S., Fernández, L. J., Sanz‐Herrera, J. A., Ochoa, I., Doweidar, M. H., & Doblaré, M. (2020) · Scientific Reports · doi:10.1038/s41598-020-78215-3 · Cited by 39 · see citing works
Jiang, G., Chen, H., Huang, J., Song, Q., Chen, Y., Gu, X. Q., Zhen-huan, J., Huang, Y., Lin, Y., Feng, J., et al. (2020) · Advanced Science · doi:10.1002/advs.201903290 · Cited by 38 · see citing works
Review: 3D cell models for organ-on-a-chip applications
Żuchowska, A., Baranowska, P., Flont, M., Brzózka, Z., & Jastrzębska, E. (2024) · Analytica Chimica Acta · doi:10.1016/j.aca.2024.342413 · Cited by 38 · see citing works
Tissue‐Engineered Microvessels: A Review of Current Engineering Strategies and Applications
Zhao, N., Pessell, A. F., Zhu, N., & Searson, P. C. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202303419 · Cited by 37 · see citing works
Pun, S., Prakash, A., Demaree, D., Krummel, D. P., Sciumè, G., Sengupta, S., & Barrile, R. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202401876 · Cited by 36 · see citing works
Ustun, M., Dabbagh, S. R., Ilci, I., Onder, T. B., & Taşoğlu, S. (2021) · Micromachines · doi:10.3390/mi12050490 · Cited by 37 · see citing works
ZNF117 regulates glioblastoma stem cell differentiation towards oligodendroglial lineage
Liu, J., Wang, X., Chen, A. T., Gao, X., Himes, B. T., Zhang, H., Chen, Z., Wang, J., Sheu, W. C., Deng, G., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29884-3 · Cited by 36 · see citing works
Self-citationThenuwara, G., Javed, B., Singh, B., & Tian, F. (2024) · Sensors · doi:10.3390/s24092865 · Cited by 35 · see citing works
Ngo, M. T., Sarkaria, J. N., & Harley, B. A. C. (2022) · Advanced Science · doi:10.1002/advs.202201888 · Cited by 34 · see citing works
Luque‐González, M. A., Reis, R. L., Kundu, S. C., & Caballero, D. (2020) · Advanced Biosystems · doi:10.1002/adbi.202000045 · Cited by 34 · see citing works
TME-targeted approaches of brain metastases and its clinical therapeutic evidence
Khan, I. M., Khan, S. U., Sala, H. S. S., Khan, M. U., Din, M. A. U., Khan, S., Hassan, S. S. U., Khan, N. M., & Liu, Y. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1131874 · Cited by 31 · see citing works
On-chip modeling of tumor evolution: Advances, challenges and opportunities
Li, C., Holman, J. B., Shi, Z., Qiu, B., & Ding, W. (2023) · Materials Today Bio · doi:10.1016/j.mtbio.2023.100724 · Cited by 32 · see citing works
Precision oncology using ex vivo technology: a step towards individualised cancer care?
Williams, S. T., Wells, G., Conroy, S., Gagg, H., Allen, R. J., Rominiyi, O., Helleday, T., Hullock, K., Pennington, C. E. W., Rantala, J., et al. (2022) · Expert Reviews in Molecular Medicine · doi:10.1017/erm.2022.32 · Cited by 32 · see citing works
Recent Developments in Glioblastoma‐On‐A‐Chip for Advanced Drug Screening Applications
Maity, S., Bhuyan, T., Jewell, C., Kawakita, S., Sharma, S., Nguyen, H. T., Najafabadi, A. H., Ermis, M., Falcone, N., Chen, J., et al. (2024) · Small · doi:10.1002/smll.202405511 · Cited by 31 · see citing works
Liu, F., Peng, B., Li, M., Ma, J., Deng, G., Zhang, S., Sheu, W. C., Zou, P., Wu, H., Liu, J., et al. (2021) · Cell Reports Physical Science · doi:10.1016/j.xcrp.2021.100691 · Cited by 30 · see citing works
Self-citationWang, R., Zhang, C., Li, D., & Yao, Y. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.1057913 · Cited by 30 · see citing works
Glioblastoma mechanobiology at multiple length scales
Kondapaneni, R. V., Gurung, S. K., Nakod, P. S., Goodarzi, K., Yakati, V., Lenart, N. A., & Rao, S. S. (2024) · Biomaterials Advances · doi:10.1016/j.bioadv.2024.213860 · Cited by 26 · see citing works
Ugodnikov, A., Persson, H., & Simmons, C. A. (2024) · Lab on a Chip · doi:10.1039/d3lc01027a · Cited by 29 · see citing works
A Scaffold-Free 3-D Co-Culture Mimics the Major Features of the Reverse Warburg Effect In Vitro
Keller, F., Bruch, R., Schneider, R., Meier-Hubberten, J. C., Hafner, M., & Rudolf, R. (2020) · Cells · doi:10.3390/cells9081900 · Cited by 24 · see citing works
Development of Tumor-Vasculature Interaction on Chip Mimicking Vessel Co-Option of Glioblastoma
Bae, J., Kim, M., Han, S., & Park, S. (2022) · BioChip Journal · doi:10.1007/s13206-022-00090-z · Cited by 25 · see citing works
The Applications and Challenges of the Development of In Vitro Tumor Microenvironment Chips
Johnson, A., Reimer, S., Childres, R., Cupp, G., Kohs, T. C. L., McCarty, O. J. T., & Kang, Y. B. (2022) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-022-00755-7 · Cited by 24 · see citing works
Hill, L. K., Bruns, J., & Zustiak, S. P. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.05.005 · Cited by 24 · see citing works
Piantino, M., Figarol, A., & Matsusaki, M. (2021) · Frontiers in Toxicology · doi:10.3389/ftox.2021.656254 · Cited by 24 · see citing works
Use and application of organ-on-a-chip platforms in cancer research
Yu, Y., Zhou, T., & Cao, L.-L. (2023) · Journal of Cell Communication and Signaling · doi:10.1007/s12079-023-00790-7 · Cited by 25 · see citing works
Rattray, Z., Deng, G., Zhang, S., Shirali, A. R., May, C., Chen, X., Cuffari, B. J., Liu, J., Zou, P., Rattray, N. J. W., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.145875 · Cited by 22 · see citing works
Self-citationSong, J., Bang, S., Choi, N., & Kim, H. N. (2022) · Biomicrofluidics · doi:10.1063/5.0121476 · Cited by 23 · see citing works
Fei, X., Wu, J., Tian, H., Jiang, D., Chen, H., Yan, K., Wang, Y., Zhao, Y., Chen, H., Xie, X., et al. (2024) · Cancer Biomarkers · doi:10.3233/cbm-230486 · Cited by 20 · see citing works
Bang, S., Tahk, D., Choi, Y. H., Lee, S., Lim, J., Lee, B., Kim, B., Kim, H. N., Hwang, N. S.-Y., & Jeon, N. L. (2021) · Advanced Functional Materials · doi:10.1002/adfm.202105475 · Cited by 19 · see citing works
A Microfluidic Organ-On-A-Chip: Into the Next Decade of Bone Tissue Engineering Applied in Dentistry
Syahruddin, M. H., Anggraeni, R., & Ana, I. D. (2023) · Future Science OA · doi:10.2144/fsoa-2023-0061 · Cited by 19 · see citing works
Microphysiological systems for human aging research
Park, S., Laskow, T. C., Chen, J., Guha, P., Dawn, B., & Kim, D. (2024) · Aging Cell · doi:10.1111/acel.14070 · Cited by 20 · see citing works
Self-citationPhenocopying Glioblastoma: A Review
Oraiopoulou, M., Tzamali, E., Papamatheakis, J. D., & Sakkalis, V. (2021) · IEEE Reviews in Biomedical Engineering · doi:10.1109/rbme.2021.3111744 · Cited by 18 · see citing works
Amemiya, T., Hata, N., Mizoguchi, M., Yokokawa, R., Kawamura, Y., Hatae, R., Sangatsuda, Y., Kuga, D., Fujioka, Y., Takigawa, K., et al. (2021) · Molecular Biology Reports · doi:10.1007/s11033-020-06061-7 · Cited by 18 · see citing works
Advances in the application of colorectal cancer organoids in precision medicine
Zhang, Y., Meng, R., Sha, D., Gao, H., Wang, S., Zhou, J., Wang, X., Li, F., Li, X., & Song, W. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1506606 · Cited by 17 · see citing works
Self-citationAdvanced Microfluidics for Single Cell‐Based Cancer Research
Carneiro, A., Palomer, M. A., Esteves, M., Rodrigues, C., Fernandes, J. M., Oliveira, F. A. D. S. D. S., Teixeira, A., Honrado, C., Diéguez, L., Abalde‐Cela, S., et al. (2025) · Advanced Science · doi:10.1002/advs.202500975 · Cited by 17 · see citing works
Ngo, H. T., Amartumur, S., Tran, V. T. A., Tran, M., Diep, Y. N., Cho, H., & Lee, L. P. (2023) · Biosensors · doi:10.3390/bios13020231 · Cited by 15 · see citing works
Vascular microphysiological systems (MPS): biologically relevant and potent models
Breuil, L., Kitada, A., Yadav, S., Zhou, H., Fujimoto, K., & Yokokawa, R. (2025) · Lab on a Chip · doi:10.1039/d5lc00014a · Cited by 15 · see citing works
Samantasinghar, A., Sunildutt, N., Ahmed, F., Memon, F. H., Kang, C.-U., & Choi, K. H. (2025) · ACS Omega · doi:10.1021/acsomega.4c11227 · Cited by 15 · see citing works
Chuaychob, S., Lyu, R., Tanaka, M., Haginiwa, A., Kitada, A., Nakamura, T., & Yokokawa, R. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2312472121 · Cited by 13 · see citing works
Multi-scale cellular engineering: From molecules to organ-on-a-chip
Huang, N. F., Chaudhuri, O., Cahan, P., Wang, A., Engler, A. J., Wang, Y., Kumar, S., Khademhosseini, A., & Li, S. (2020) · APL Bioengineering · doi:10.1063/1.5129788 · Cited by 14 · see citing works
Flow‐Induced Vascular Remodeling on‐Chip: Implications for Anti‐VEGF Therapy
Mirzapourshafiyi, F., Huber, E., Karr, L., Tong, J., Bausch, A. R., Simmel, F. C., & Alim, K. (2025) · Advanced Functional Materials · doi:10.1002/adfm.202501416 · Cited by 12 · see citing works
Microphysiological systems to study tumor-stroma interactions in brain cancer
Neves, E. R., Harley, B. A. C., & Pedrón, S. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.06.012 · Cited by 12 · see citing works
Considerations for modelling diffuse high-grade gliomas and developing clinically relevant therapies
Higginbottom, S. L., Tomaskovic‐Crook, E., & Crook, J. M. (2023) · Cancer and Metastasis Reviews · doi:10.1007/s10555-023-10100-7 · Cited by 11 · see citing works
Recapitulating the Cancer‐Immunity Cycle on a Chip
Lee, Y., Min, J., Kim, S., Park, W., Ko, J., & Jeon, N. L. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202401927 · Cited by 10 · see citing works
Cross-platform analysis reveals cellular and molecular landscape of glioblastoma invasion
Chen, A. T., Xiao, Y., Tang, X., Baqri, M., Gao, X., Reschke, M., Sheu, W. C., Long, G., Zhou, Y., Deng, G., et al. (2022) · Neuro-Oncology · doi:10.1093/neuonc/noac186 · Cited by 10 · see citing works
Self-citationGlioma nanomedicine: Design, fabrication and theranostic application
Wu, D., Zhao, J., Xu, T., Xiang, H., Zhao, B., Gao, L., & Chen, Y. (2024) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2024.215696 · Cited by 9 · see citing works
Moghaddam, F. D., Rafiee, M., Setayeshfar, A., Moradi, A., Esmaeili, Y., Bertani, F. R., Neisiany, R. E., You, Z., & Zare, E. N. (2024) · Advanced Materials Technologies · doi:10.1002/admt.202400134 · Cited by 9 · see citing works
Microfabricated Organ-Specific Models of Tumor Microenvironments
Oh, J. M., Park, Y., Lee, J., & Shen, K. (2025) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-110222-103522 · Cited by 9 · see citing works
Parihar, P., Sunildutt, N., Rahim, C. S. A., Samantasinghar, A., Lim, J., & Choi, K. H. (2024) · Advanced Therapeutics · doi:10.1002/adtp.202300410 · Cited by 10 · see citing works
Biomaterials meet organ-on-chips – a perspective on tumor modeling
Monteiro, C. F., Deus, I. A., Custódio, C. A., & Mano, J. F. (2024) · International Materials Reviews · doi:10.1177/09506608241303436 · Cited by 8 · see citing works
Liang, M., Lei, F., Liu, Y., Lan, D., Huang, H., Zhang, G., Feng, Q., Cao, X., & Dong, H. (2021) · ACS Applied Bio Materials · doi:10.1021/acsabm.1c00534 · Cited by 8 · see citing works
Advances in computational and translational approaches for malignant glioma
Bhargav, A. G., Domino, J. S., Alvarado, A. M., Tuchek, C. A., Akhavan, D., & Camarata, P. J. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1219291 · Cited by 7 · see citing works
Sheidaei, Z., Akbarzadeh, P., Nguyen, N., & Kashaninejad, N. (2022) · Biomedical Microdevices · doi:10.1007/s10544-022-00615-1 · Cited by 5 · see citing works
Lungu, I. I., & Grumezescu, A. M. (2019) · Biomedical Engineering International · doi:10.33263/biomed11.002008 · Cited by 5 · see citing works
Bridging the Gap: How Organ‐on‐a‐Chip Technology Facilitates the Battle against Glioma
Liu, S., Gong, Z., Zhou, D., Ayala‐Nunez, V., Xu, T., & Wick, P. (2025) · Small Science · doi:10.1002/smsc.202500154 · Cited by 5 · see citing works
MEMS in Twenty-First-Century Healthcare
Noushin, T., Parvez, M. S., Biswas, P., Bhuiyan, M. E. H., Rumon, M. A. A., & Tabassum, S. (2025) · Springer tracts in electrical and electronics engineering · doi:10.1007/978-981-96-4659-3_3 · Cited by 5 · see citing works
Mares, A. G., Feiner‐Gracia, N., Muela, Y., Martínez, G., Delgado, L., Albertazzi, L., & Pujals, S. (2021) · Applied Nano · doi:10.3390/applnano2040021 · Cited by 4 · see citing works
Perspective of using in vitro models to understand immunotherapy-induced cytokine release syndrome
Perkins, E., Cooper, C., Lund, E., Alb, M., Morgan, H., Fogal, B., Hewitt, P. G., Mazein, A., Ostaszewski, M., & Sewald, K. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1732193 · Cited by 4 · see citing works
Ding, L.-Y., Chang, C., Chen, S.-Y., Chen, K.-L., Li, Y.-S., Wu, Y. R., Hsu, T.-Y., Ying, H.-Y., Wu, H., Hughes, M. W., et al. (2024) · American Journal Of Pathology · doi:10.1016/j.ajpath.2024.02.023 · Cited by 3 · see citing works
Kim, S., Park, S.-J., Chowdhury, T., Hong, J.-I., Ahn, J., Jeong, T. Y., Yu, H. J., Shin, Y., Ku, J., Park, J. B., et al. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04188-3 · Cited by 2 · see citing works
Alshabi, A. H. A., Qardash, A. A. A., & Hafez, A. I. A. (2023) · المجلة العلمية للدراسات التجارية والبيئية · doi:10.21608/jces.2023.304473 · Cited by 1 · see citing works
Understanding Glioblastoma Dynamics Using 3D Organoids and Engineered Extracellular Matrix
McManis, A., Jimenez, C. A., Shirolkar, A., Rehman, S. R. U., Mallick, S., Murphy, M. M., Gaharwar, A. K., & Singh, I. (2026) · Advanced Science · doi:10.1002/advs.202522926 · Cited by 1 · see citing works
On-chip perivascular niche with patient-derived glioma cellsPreprint
Gerigk, M., Bulstrode, H. J. C. J., Shi, H., Tönisen, F., Cerutti, C., Morrison, G. M., Rowitch, D. H., & Huang, Y. Y. S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.23.424179 · Cited by 1 · see citing works
Ngo, M. T., Sarkaria, J. N., & Harley, B. A. C. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.27.489740 · Cited by 1 · see citing works
- Authors
- Xiao, Y., Kim, D., Dura, B., Zhang, K., Yan, R., Li, H., Han, E., Ip, J., Zou, P., Liu, J., Chen, A. T., Vortmeyer, A. O., Zhou, J., & Fan, R.
- Affiliations
- Yale University (US)
- Carnegie Mellon University (US)
- Indiana University Health (US)
- Yale Cancer Center (US)
- Corresponding author
- Fan, Rong
- ORCID
- Venue
- Advanced Science
- Publisher
- Wiley
- Published
- 2019-02-10
- Volume
- 6
- Issue
- 8
- Pages
- 1801531-1801531
- ISSN
- 2198-3844 (ISSN-L)
- PMC
- PMC6468969
- OpenAlex
- W2913629863
- Cited by
- 115
- References
- 83
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 20 · 2023: 15 · 2022: 20 · 2021: 21 · 2020: 15 · 2019: 3
- FWCI
- 8.08
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Advanced Science (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- IUScholarWorks (Indiana University) (submittedVersion, cc-by)
- Publisher
- Funders
- National Science Foundation (CBET‐1351443)
- National Cancer Institute (U54 CA193461, U54 CA209992)
- National Institutes of Health (R01 NS095817)
- Topics
- Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Keywords
- glioblastoma, perivascular niche, tumor heterogeneity, tumor cell migration, tumor cell subtypes, proneural subtype, mesenchymal subtype, PDGFRA, single-cell transcriptomics
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